Yansu LIU,Jiangyan SHEN,Ke FANG,et al.Behavior and Approximate Entropy of Right-eye Lateralization During Predation in the Music Frog[J].Asian Herpetological Research(AHR),2020,11(2):115-123.[doi:10.16373/j.cnki.ahr.190049]
Click Copy

Behavior and Approximate Entropy of Right-eye Lateralization During Predation in the Music Frog
Share To:

Asian Herpetological Research[ISSN:2095-0357/CN:51-1735/Q]

2020 VoI.11 No.2
Research Field:
Publishing date:


Behavior and Approximate Entropy of Right-eye Lateralization During Predation in the Music Frog
Yansu LIU1 Jiangyan SHEN2 Ke FANG3 Jinjin SONG3 Yanzhu FAN2 Jing YANG2 Di SHEN2 Fang LU4* and Guangzhan FANG2*
1 Sichuan Nursing Vocational College, Chengdu 610100, Sichuan, China
2 Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, Sichuan, China
3 School of Life Science, Anhui University, Hefei 230601, Anhui, China
4 Department of Ophthalmology, West China Hospital, Sichuan University, Chengdu 610041, Sichuan, China
approximate entropy (ApEn) complexity electroencephalogram (EEG) frog lateralization predatory behavior right-eye preference
Brain asymmetry for processing visual information is widespread in animals. However, it is still unknown how the complexity of the underlying neural network activities represents this asymmetrical pattern in the brain. In the present study, we investigated this complexity using the approximate entropy (ApEn) protocol for electroencephalogram (EEG) recordings from the forebrain and midbrain while the music frogs (Nidirana daunchina) attacked prey stimulus. The results showed that (1) more significant prey responses were evoked by the prey stimulus presented in the right visual field than that in the left visual field, consistent with the idea that right-eye preferences for predatory behaviors exist in animals including anurans; (2) in general, the ApEn value of the left hemisphere (especially the left mesencephalon) was greatest under various stimulus conditions, suggesting that visual lateralization could be reflected by the dynamics of underlying neural network activities and that the stable left-hemisphere dominance of EEG ApEn may play an important role in maintaining this brain asymmetry.


Andrew R. J. 1983. Lateralization of emotional and cognitive function in higher vertebrates, with special reference to the domestic chick. In Ewert J. P. , Capranica R. R., Ingle D. J. (Eds.) Advances in vertebrate neuroethology. New York: Plenum. 477–509
Andrew R. J. 2002. The earliest origins and subsequent evolution of lateralization. In Rogers L. J., Andrew R. J. (Eds.) Comparative vertebrate lateralization. Cambridge: Cambridge University Press. 70–93
Andrew R. J., Mench J., Rainey C. 1982. Right-left asymmetry of response to visual stimuli in the domestic chick. In Ingle D., Goodale M. A., Mansfield R. J. W. (Eds.) Analysis of visual behaviour. Cambridge: MIT Press. 197–209
Andrew R. J., Rogers L. J. 2002. The nature of lateralization in tetrapods. In Rogers L. J., Andrew R. J. (Eds.) Comparative vertebrate lateralization. Cambridge: Cambridge University Press. 94–125
Ariyomo T. O., Watt P. J. 2013. Aggression and sex differences in lateralization in the zebrafish. Anim Behav, 86(3): 617–622
Babcock L. E. 1993. Trilobite malformations and the fossil record of behavioral asymmetry. J Paleont, 67(2): 217–229
Babloyantz A., Salazar J., Nicolis C. 1985. Evidence of chaotic dynamics of brain activity during the sleep cycle. Phys lett A, 111(3): 152–156
Bassett D. S., Gazzaniga M. S. 2011. Understanding complexity in the human brain. Trends Cogn Sci, 15(5): 200–209
Besson M., Gache C., Bertucci F., Brooker R. M., Roux N., Jacob H., Berthe C., Sovrano V. A., Dixson D. L., Lecchini D. 2017. Exposure to agricultural pesticide impairs visual lateralization in a larval coral reef fish. Sci Rep, 7(1): 9165
Bianki V. L. 2014. Sex differences in lateralization in the animal brain. Amsterdam: Harwood Academic Publishers
Bibost A. L., Kydd E., Brown C. 2013. The effect of sex and early environment on the lateralization of the rainbowfish Melanotaenia duboulayi. In Csermely D., Regolin L. (Eds.) Behavioral lateralization in vertebrates. Heidelberg: Springer. 9–24
Bisazza A., Cantalupo C., Capocchiano M., Vallortigara G. 2000. Population lateralisation and social behaviour: A study with 16 species of fish. Laterality, 5(3): 269–284
Bisazza A., Dadda M. 2005. Enhanced schooling performance in lateralized fishes. Proc R Soc B: Biol Sci, 272(1573): 1677–1681
Bisazza A., Pignatti R., Vallortigara G. 1997. Detour tests reveal task-and stimulus-specific behavioural lateralization in mosquitofish (Gambusia holbrooki). Behav Brain Res, 89(1–2): 237–242
Bizas E., Simos P., Stam C., Arvanitis S., Terzakis D., Micheloyannis S. 1999. EEG correlates of cerebral engagement in reading tasks. Brain Topogr, 12(2): 99–105
Bonati B., Csermely D., Romani R. 2008. Lateralization in the predatory behaviour of the common wall lizard (Podarcis muralis). Behav Process, 79(3): 171–174
Bonati B., Csermely D., Sovrano V. A. 2013. Advantages in exploring a new environment with the left eye in lizards. Behav Process, 97: 80–83
Bradshaw J., Rogers L. 1992. The evolution of lateral asymmetries, language, tool use, and intellect. San Diego: Academic Press
Burghagen H., Ewert J. P. 1983. Influence of the background for discriminating object motion from self-induced motion in toads Bufo bufo (L.). J Comp Physiol, 152(2): 241–249
Dimond S. J., Farrington L., Johnson P. 1976. Differing emotional response from right and left hemispheres. Nature, 261(5562): 690–692
Güntürkün O., Diekamp B., Manns M., Nottelmann F., Prior H., Schwarz A., Skiba M. 2000. Asymmetry pays: Visual lateralization improves discrimination success in pigeons. Curr Biol, 10(17): 1079–1081
Heuts B. 1999. Lateralization of trunk muscle volume, and lateralization of swimming turns of fish responding to external stimuli. Behav Process, 47(2): 113–124
Hogan M. J., Kilmartin L., Keane M., Collins P., Staff R. T., Kaiser J., Lai R., Upton N. 2012. Electrophysiological entropy in younger adults, older controls and older cognitively declined adults. Brain Res, 1445: 1–10
Hook-Costigan M. A., Rogers L. J. 1998. Eye preferences in common marmosets (Callithrix jacchus): Influence of age, stimulus, and hand preference. Laterality, 3(2): 109–130
Inouye T., Shinosaki K., Iyama A., Matsumoto Y. 1993. Localization of activated areas and directional EEG patterns during mental arithmetic. Electroencephalogr Clin Neurophysiol, 86(4): 224–230
Inouye T., Shinosaki K., Sakamoto H., Toi S., Ukai S., Iyama A., Katsuda Y., Hirano M. 1991. Quantification of EEG irregularity by use of the entropy of the power spectrum. Electroencephalogr Clin Neurophysiol, 79(3): 204–210
Jeong J. 2004. EEG dynamics in patients with Alzheimer’s disease. Clin Neurophysiol, 115(7): 1490–1505
Jozet-Alves C., Viblanc V. A., Romagny S., Dacher M., Healy S. D., Dickel L. 2012. Visual lateralization is task and age dependent in cuttlefish, Sepia officinalis. Anim Behav, 83(6): 1313–1318
Koboroff A., Kaplan G., Rogers L. J. 2008. Hemispheric specialization in Australian magpies (Gymnorhina tibicen) shown as eye preferences during response to a predator. Brain Res Bull, 76(3): 304–306
Letzkus P., Boeddeker N., Wood J. T., Zhang S. W., Srinivasan M. V. 2008. Lateralization of visual learning in the honeybee. Biol Lett, 4(1): 16–19
Li X., Jiang Y., Hong J., Dong Y. Z., Yao L. 2016. Estimation of cognitive workload by approximate entropy of EEG. J Mech Med Biol, 16(06): 1650077
Lippé S., Kovacevic N., McIntosh R. 2009. Differential maturation of brain signal complexity in the human auditory and visual system. Front Hum Neurosci, 3: 48
Liu Y. S., Fan Y. Z., Xue F., Yue X. Z., Brauth S. E., Tang Y. Z., Fang G. Z. 2016. Changes in electroencephalogram approximate entropy reflect auditory processing and functional complexity in frogs. Asian Herpetol Res, 7(3): 180–190
Magat M., Brown C. 2009. Laterality enhances cognition in Australian parrots. Proc R Soc B: Biol Sci, 276(1676): 4155–4162
Martín J., López P., Bonati B., Csermely D. 2010. Lateralization when monitoring predators in the wild: A left eye control in the common wall lizard (Podarcis muralis). Ethology, 116(12): 1226–1233
McGrew W., Marchant L. 1999. Laterality of hand use pays off in foraging success for wild chimpanzees. Primates, 40(3): 509–513
Micheloyannis S., Papanikolaou E., Bizas E., Stam C. J., Simos P. G. 2002. Ongoing electroencephalographic signal study of simple arithmetic using linear and non-linear measures. Int J Psychophysiol, 44(3): 231–238
Namazi H., Khosrowabadi R., Hussaini J., Habibi S., Farid A. A., Kulish V. V. 2016. Analysis of the influence of memory content of auditory stimuli on the memory content of EEG signal. Oncotarget, 7(35): 56120–56128
Pascual A., Huang K. L., Neveu J., Préat T. 2004. Neuroanatomy: Brain asymmetry and long-term memory. Nature, 427(6975): 605–606
Pincus S. 1995a. Approximate entropy (ApEn) as a complexity measure. Chaos, 5(1): 110–117
Pincus S. M. 1991. Approximate entropy as a measure of system complexity. Proc Natl Acad Sci USA, 88(6): 2297–2301
Pincus S. M. 1995b. Quantifying complexity and regularity of neurobiological systems Methods in Neurosciences No. 28. Academic Press. 336–363
Quaresmini C., Forrester G. S., Spiezio C., Vallortigara G. 2014. Social environment elicits lateralized behaviors in gorillas (Gorilla gorilla gorilla) and chimpanzees (Pan troglodytes). J Comp Psychol, 128(3): 276–284
Reddon A. R., Hurd P. L. 2008. Aggression, sex and individual differences in cerebral lateralization in a cichlid fish. Biol Lett, 4(4): 338–340
Robins A., Rogers L. J. 2004. Lateralized prey-catching responses in the cane toad, Bufo marinus: Analysis of complex visual stimuli. Anim Behav, 68(4): 767–775
Robins A., Rogers L. J. 2006a. Complementary and lateralized forms of processing in Bufo marinus for novel and familiar prey. Neurobiol Learn Mem, 86(2): 214–227
Robins A., Rogers L. J. 2006b. Lateralized visual and motor responses in the green tree frog, Litoria caerulea. Anim Behav, 72(4): 843–852
Rogers L. J. 2002. Lateralised brain function in anurans: Comparison to lateralisation in other vertebrates. Laterality, 7(3): 219–239
Rogers L. J., Vallortigara G., Andrew R. J. 2013. Divided brains: The biology and behaviour of brain asymmetries. Cambridge, UK: Cambridge University Press
Rogers L. J., Zucca P., Vallortigara G. 2004. Advantages of having a lateralized brain. Proc R Soc Lond B Biol Sci, 271(Suppl 6): S420–S422
Schnell A. K., Hanlon R. T., Benkada A., Jozet-Alves C. 2016. Lateralization of eye use in cuttlefish: Opposite direction for anti-predatory and predatory behaviors. Front Physiol, 7: 620
Shen J. Y., Fang K., Fan Y. Z., Song J. J., Yang J., Shen D., Liu Y. S., Fang G. Z. 2019. Dynamics of electroencephalogram oscillations underlie right-eye preferences in predatory behavior of the music frog. J Exp Biol, 222(22): jeb212175
Sporns O. 2002. Network analysis, complexity, and brain function. Complexity, 8(1): 56–60
Sporns O., Tononi G., Edelman G. M. 2000. Connectivity and complexity: The relationship between neuroanatomy and brain dynamics. Neural Networks, 13(8–9): 909–922
Stam C. J. 2005. Nonlinear dynamical analysis of EEG and MEG: Review of an emerging field. Clin Neurophysiol, 116(10): 2266–2301
Talebi N., Nasrabadi A. M., Curran T. 2012. Investigation of changes in EEG complexity during memory retri: The effect of midazolam. Cogn Neurodyn, 6(6): 537–546
Thieltges H., Lemasson A., Kuczaj S., B?ye M., Blois-Heulin C. 2011. Visual laterality in dolphins when looking at (un) familiar humans. Anim Cogn, 14(2): 303–308
Tomberg C. 1999. Focal enhancement of chaotic strange attractor dimension in the left semantic (Wernicke) human cortex during reading without concomitant change in vigilance level. Neurosci Lett, 263(2): 177–180
Tononi G., Edelman G. M. 1998. Consciousness and complexity. Science, 282(5395): 1846–1851Wachowitz S., Ewert J. P. 1996. A key by which the toad’s visual system gets access to the domain of prey. Physiol Behav, 60(3): 877–887
Yue X. Z., Fan Y. Z., Xue F., Brauth S. E., Tang Y. Z., Fang G. Z. 2017. The first call note plays a crucial role in frog vocal communication. Sci Rep, 7(1): 10128
Zarjam P., Epps J., Chen F., Lovell N. H. 2013. Estimating cognitive workload using wavelet entropy-based features during an arithmetic task. Comput Biol Med, 43(12): 2186–2195


Last Update: 2020-06-25